Association of hydromyelia and acute compressive myelopathy caused by intervertebral disc extrusion in dogs

Abstract Background Hydromyelia is a common magnetic resonance imaging (MRI) finding associated with compressive myelopathy caused by intervertebral disc extrusion (IVDE). Objectives To describe the MRI features of hydromyelia and explore its relationship to clinical history, neurological severity, and the duration of cord compression. Animals Ninety‐one client‐owned dogs with a focal compressive myelopathy secondary to thoracolumbar IVDE. Methods A retrospective observational study was conducted in which MRIs were blindly evaluated to grade and localize hydromyelia and measure the degree of spinal cord compression. Duration and severity of clinical signs were recorded. Differences between hydromyelia grades in these variables were statistically assessed using a Wilcoxon and Kruskal Wallis test. Receiver operator curve analysis was used to determine the sensitivity and specificity for duration of clinical signs to predict the presence of hydromyelia. Results Hydromyelia was identified at sites of IVDE in 84 of 91 dogs. An absence of hydromyelia was associated a with statistically longer duration of clinical signs (mean 73.1, IQR 76 days) when compared to cases with mild (mean 17.7, IQR 7.25 days, P = .006) or severe (mean 17.9, IQR 10.25 days, P = .006) hydromyelia. Duration of clinical signs <14 days was 78.6% sensitive and 85.7% specific for predicting the presence of hydromyelia. Conclusions and Clinical Importance The MRI finding of hydromyelia might be a predictor of lesion chronicity in focal IVDE, helping to guide planning of hemilaminectomy surgery.


| INTRODUCTION
Intervertebral disc extrusion (IVDE) and secondary compressive myelopathy is the most common cause for spinal cord injury in dogs, 1,2 representing 2.3% of all admissions into veterinary teaching hospitals. 3 Extruded intervertebral disc material and hemorrhage causes attenuation of the spinal canal and variable degrees of spinal cord injury including compression, edema, necrosis, hemorrhage, and contusion. 4 This spinal cord injury can cause profound neurological dysfunction that commonly results in the need for urgent decompressive laminectomy.
The mainstay for diagnosis of IVDE is magnetic resonance imaging (MRI). This modality has the contrast resolution to detect displacement of disc material, confirm the location of spinal cord compression and assess the degree of spinal cord injury. The MRI features of acute IVDE have been well documented 5,6 and multiple different variables have been assessed to identify MRI features that can predict neurological status and prognosis, including degree of cord compression, spinal cord hyperintensity and loss of subarachnoid signal. [7][8][9] There is a lack of information describing the MRI appearance of more chronic lesions. 10 This lack of predictive MRI features for lesion chronicity limits our ability to differentiate between sites of chronic and acute extrusion, a necessary part of surgical planning in dogs with IVDE.
The presence of hydromyelia is a potential indicator of IVDE chronicity. Hydromyelia is the distension of the ependymal lined central canal that communicates with the ventricular system. 11 This is different from syringohydromyelia, where there is extension of the fluid through the ependymal lining and cavity formation within the spinal cord parenchyma, a feature that is not associated with IVDE histopathologically. 4,12 In the normal canine spinal cord, the central canal measures approximately 0.03 mm in diameter and is either undetectable or only minimally visible on sagittal and transverse T2-weighted sequences; however, when hydromyelia is present the central canal distends and on good quality MRI images, becomes clearly visible centrally within the cord. 13 The authors have identified that hydromyelia is a common feature of acute IVDE and likely to be related to the CSF flow disturbance caused by cord compression.
However, at sites of chronic cord compression the authors have found that hydromyelia is often not present.
In this study, we investigate the presence of hydromyelia in the setting of focal thoracolumbar IVDE. We aim to characterize the MRI features of hydromyelia in a large cohort of dogs and statistically evaluate for any correlation between hydromyelia and duration of historic clinical signs, degree of cord compression and severity of neurological status.

| Case search
The picture archiving and communication system from the Cornell University Hospital for Animals was searched for cases that had undergone thoracolumbar MRI between October 2017 and September 2021 and had a diagnosis of a focal compressive IVDE in the T3-L3 region. In addition, in order to increase the number of dogs with more chronic clinical signs, the Cornell University Hospital for Animals radiographic reports system was searched for cases with chronic thoracolumbar disc extrusions from January 2011 to October 2017.

| Inclusion criteria
All included cases were required to have a single focal IVDE causing attenuation of the vertebral canal in the T3-L3 region of the vertebral column. An extrusion was classified as displacement of intervertebral disc material to overlap the adjacent endplate or the displaced material had a height greater than its width. Cases needed to have a diagnostic quality sagittal T2-weighted sequence with a transverse T2-weighted sequence that spanned the site of IVDE and included the entirety of the abnormal region between sites of non-compressed normal spinal cord. A complete medical history and a neurological examination before MRI were also required for inclusion.

| Exclusion criteria
Cases were excluded if there was relevant artifact that impacted image quality or insufficient transverse slices to evaluate the spinal cord cranial and caudal to the site of extrusion. In order to keep the cohort as homogeneous as possible, cases were excluded if they had extruded material or hemorrhage that spanned >2 vertebral lengths, or spinal cord T2-weighted hyperintensity or spinal cord swelling that spanned >2 vertebral body lengths cranial and caudal to the site of compression. In addition, cases were excluded if they had a history of a previous confirmed disc extrusion or hemilaminectomy, had more than a single site of IVDE or exhibited evidence of concurrent primary spinal cord disease.

| Data collection
Data collected were: dog identification (number and name), signalment (age, breed, sex), date of MRI and site of IVDE. The duration of neurological signs observed before MRI was also recorded. The neurological examination was reviewed and a simple grading system utilized to score the neurological status of each case at the time of MRI [graded as the following; spinal pain only (1), paraparesis (2), paraplegia (3) or deep pain negative (4).

| MRI evaluation
Imaging was performed on a 1.5-T Toshiba Vantage Atlas MRI unit.
All studies included sagittal and transverse T2-weighted MRI sequences that spanned the site of IVDE (MRI sequence variables are documented in Table 1). Sagittal and transverse T2-weighted MR images were independently blindly reviewed by an ECVDI-certified radiologist and ACVR resident in training for the presence or absence of hydromyelia cranial and caudal to the site of spinal compression.
The location of the hydromyelia in relation to the site of compression was recorded (only cranial, only caudal, or cranial and caudal to the site of cord compression). The degree of hydromyelia was graded as absent (0), mild (1; segmental central canal distension was mild, inconsistently visible on sequential transverse slices or short in length [<2 vertebral lengths]) and severe (2; segmental central canal distension clearly visible on sequential transverse slices or long in length [>2 vertebral lengths]) and cases were grouped according to these grades.
Where disagreement was found, a consensus was formed. The crosssectional area (CSA) of spinal cord was measured by a single observer at the site of maximal compression and 1 vertebral length caudal to the site of compression, and a cord compression ratio calculated (CSA of the normal cord/CSA area of the compressed cord; Figure 1). 14

| Statistics
Histograms of the data were plotted to assess for normality.
Depending on the normality of distribution, either an ANOVA with post hoc Tukeys or a Wilcoxon with Kruskal-Wallis testing was applied to evaluate for statistically significant differences between groups with absent, mild, and severe hydromyelia for the continuous variables of; cord compression ratio, neurological severity grade and duration of clinical signs. In order to assess if duration of clinical signs could predict the presence or absence of hydromyelia on an MRI, a receiver operator curve (ROC) was generated; area under the curve was calculated and sensitivity and specificity determined for the most appropriate threshold.

| Duration of clinical signs
The  Figure 5).

| Degree of neurological dysfunction
Two dogs presented for spinal pain alone, 58 dogs presented with paraparesis, 27 presented with paraplegia, and 4 were deep pain negative. No statistically significant difference in neurological severity grade was identified between absent, mild, and severe hydromyelia groups ( Figure 4).

| Degree of spinal cord compression
The spinal cord compression ratio was not statistically significantly different between cords without hydromyelia (0.69 ± 0.07), with mild hydromyelia (0.62 ± 0.03) and with severe hydromyelia (0.58 ± 0.02; Figure 4). We made the presumption that the canal distension observed on MRI in this study is hydromyelia and not syringohydromyelia. Syrinx

| DISCUSSION
formation is a condition that should be readily visible on histopathology as cavitation within the spinal cord and, as it has not been described as a common component of IVDE histopathologically, is unlikely to be the cause for the MRI changes we describe in this study. 11,12 Central canal distension has also not been described on histopathology of IVDE. During removal of the spinal cord the pressures within the central canal will reduce, likely making the hydromyelia that we observe in-vivo inapparent on histopathology. These similar pressure-related changes should not influence the presence of a syrinx in the same way. Despite this reasoning, without histopathological confirmation of each case, the precise cause for the MRI changes described in this study cannot be completely confirmed.
Although hydromyelia has not been described in histopathology or MRI descriptions of IVDE, previous work on myelography of IVDE has observed positive contrast to fill the central canal in a subset of cases. These "canalograms" are observed as a fine (<1 mm diameter) centrally located line within the spinal cord adjacent to sites of spinal cord compression. 18,19 The central canal highlighted in these "canalograms" is enlarged when compared to what is described in normal dogs and therefore likely represent sites of hydromyelia. 13,18,19 They also visually appear similar to the distended central canals described in this study. 18,19 MRI descriptions of IVDE have not identified hydromyelia as an imaging feature of IVDE. 5,6 This might be related to the fact that many Despite the need to identify MRI features that predict lesion chronicity, there is limited information available on the imaging features of chronic IVDE in dogs, with the majority of studies only documenting the chronic changes observed after decompressive surgery. 10,22 The gliosis, atrophy, and degeneration associated with chronic spinal cord compression in humans cause T2-weighted hyperintense and T1-weighted isointense intramedullary lesions on MRI. 20,21 These signal intensity changes have been described in chronic spinal cord compression secondary to cervical spondylomyelopathy in dogs. 23 Our study found that the severity of spinal cord compression was not significantly different between hydromyelia groups. This lack of association was surprising as higher degree of spinal cord compression is expected to disrupt CSF flow more and increase the incidence and severity of hydromyelia. However, our study design might have been a cause for this lack of statistical difference in our results as, although we included a total of 91 cases, only 7 of these cases did not exhibit hydromyelia. This low number could have reduced our power to detect statistically significant differences between groups for some of the variables evaluated, and future work could focus on evaluating a higher number IVDE cases that do not exhibit hydromyelia.
This study utilized a clinical data set evaluated retrospectively. As such, there was variability in the MRI sequence variables between subjects. This lack of standardization might have reduced our ability to visualize hydromyelia. In particular, slice thickness was variable in the sagittal plane sequences, potentially reducing our ability to detect hydromyelia on these sequences. For this reason, the transverse slices were used primarily for the detection of hydromyelia in all cases.
This study explored the clinical and MRI features of hydromyelia in dogs with focal thoracolumbar IVDE and compressive myelopathy.
The findings identified in this paper suggest that hydromyelia might be an MRI feature of acute IVDE and its absence could be a predictor of more chronic of IVDEs. Being able to differentiate between acute and chronic IVDE at the time of MRI is an important component of the preoperative assessment for surgical planning in dogs with IVDE.

ACKNOWLEDGMENT
No funding was received for this study.